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Completion of the life cycle of Tylodelphys mashonense (Sudarikov, 1971) (Digenea: Diplostomidae) with DNA barcodes and rDNA sequences

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Abstract

The life cycle of Tylodelphys mashonense (Digenea: Diplostomidae), whose metacercariae occur in the cranial cavity of the widely cultivated catfish Clarias gariepinus, was resolved by the application of molecular markers. Both COI barcodes and ITS sequences obtained from diplostomid-like cercariae infecting Bulinus spp. from Mindu Dam, Morogoro, matched those acquired from metacercariae from the catfish C. gariepinus, and those from adult T. mashonense from the grey heron Ardea cinerea and the white egret Egretta alba. The success in linking the life cycle stages of T. mashonense using molecular tools highlights the usefulness of this approach in resolving the complex life cycles of digeneans in the absence of experimental establishment.

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References

  • Baer JG (1957) Trématodes et cestodes récoltés en Côte d’Ivoire, avec remarques sur lafamille des Dicrocoeliidae Odhner etsur les parasites des Damans. Rev Suisse Zool 64:547–575

    Article  Google Scholar 

  • Barson M, Rodney B, Ollevier F, Huyse T (2008) Taxonomy and faunistics of the helminth parasites of Clarias gariepinus (Burchell, 1822), and Oreochromis mossambicus (Peters, 1852) from temporary pans and pools in the Save-Runde River floodplain, Zimbabwe. Comp Parasitol 75:228–240

    Article  Google Scholar 

  • Behrmann-Godel J (2013) Parasite identification, succession and infection pathways in perch fry (Perca fluviatilis): new insights through a combined morphological and genetic approach. Parasitology 140:509–520

    Article  CAS  PubMed  Google Scholar 

  • Beverley-Burton M (1963) A new strigeid Diplostomum (T) mashonensen.sp (Trematoda: Diplostomatidae) from the Grey Heron, Ardea Cinerea L., in Southern Rhodesia with an experimental demonstration of part of the life cycle. Rev Zool Bot Afr LXVIII:291–306

    Google Scholar 

  • Brown DS (2005) Freshwater snails of Africa and their medical importance, 2nd edn. Taylor & Fransis, London

    Google Scholar 

  • Chappell LH, Hardie LJ, Secombes CJ (1994) Diplostomiasis: the disease and host-parasite interactions. In: Pike AW, Lewis JW (eds) Parasitic diseases of fish. Samara Publishing Limited, Dyefed, pp 59–86

    Google Scholar 

  • Chibwana FD, Nkwengulila G (2010) Variation in the morphometrics of diplostomid metacercariae (Digenea: Trematoda) infecting the catfish, Clarias gariepinus in Tanzania. J Helminthol 84:61–70

    Article  CAS  PubMed  Google Scholar 

  • Chibwana FD, Blasco-Costa I, Georgieva S, Hosea KM, Nkwengulila G, Scholz T, Kostadinova A (2013) A first insight into the barcodes for African diplostomids (Digenea: Diplostomidae): brain parasites in Clarias gariepinus (Siluriformes: Clariidae). Infect Genet Evol 17:62–70

    Article  PubMed  Google Scholar 

  • Cribb TH, Andersona GR, Adlard RD, Bray RA (1998) A DNA-based demonstration of a three-host life-cycle for the Bivesiculidae (Platyhelminthes: Digenea). Int J Parasitol 28:680–684

    Google Scholar 

  • De Graaf G, Janssen H (1996) Artificial reproduction and pond rearing of the Arican catfish Clarias gariepinus in sub-Saharan Africa—a handbook. Food and Agricultural Organization of the United Nations, Rome

    Google Scholar 

  • El-Naffar MK (1979) Parasites of the Egyptian moorhens. I: Diplostomum magnicaudumsp. nov. with part of its life cycle. J Egypt Soc Parasitol 9:349–358

    Google Scholar 

  • El-Naffar MK, Khalifa RM, Sakla AA (1980) Parasitofauna of the Egyptian aquatic birds. II. Trematode parasites of the Giant Heron (Ardea goliath) in Assiut Governorate. J Egypt Soc Parasitol 10:107–116

  • Faltýnková A (2005) Larval trematodes (Digenea) in molluscs from small water bodies near Šeské Budšjovice, Czech Republic. Acta Parasitol 50:49–55

    Google Scholar 

  • Flores V (1997) Contribution to the morphological description of Tylodelphys barilochensis and Tylodelphys crubensis (Trematoda, Diplostomidae) encephalon parasites of Galaxias maculatus (Teleostei, Galaxiidae). Bol Chil Parasitol 52:84–8

    CAS  PubMed  Google Scholar 

  • Flores VR, Semenas LG (2008) Larval digenean community parasitizing the freshwater snail, Chilina dombeyana (Pulmonata: Chilinidae) in Patagonia, Argentina, with special reference to the notocotylid Catatropis chilinae. J Parasitol 94:305–313

    Article  PubMed  Google Scholar 

  • Galazzo DE, Dayanandan S, Marcogliese DJ, McLaughlin JD (2002) Molecular systematics of some North American species of Diplostomum (Digenea) based on rDNA-sequence data and comparisons with European congeners. Can J Zool 80:2207–2217

    Article  CAS  Google Scholar 

  • Georgieva S, Soldanova M, Perez-del-Olmo A, Dangel DR, Sitko J, Sures B, Kostadinova A (2013) Molecular prospecting for European Diplostomum (Digenea: Diplostomidae) reveals cryptic diversity. Int J Parasitol 43:57–72

    Article  CAS  PubMed  Google Scholar 

  • Hillis DM, Dixon MT (1991) Ribosomal DNA: molecular evolution and phylogenetic inference. Q Rev Biol 66:411–453

    Article  CAS  PubMed  Google Scholar 

  • King PH, Van As JG (1997) Description of the adult and larval stages of Tylodelphys xenopi (Trematoda: Diplostomidae) from Southern Africa. J Parasitol 83:287–295

    Article  CAS  PubMed  Google Scholar 

  • Kristensen TK (1987) A field guide to African freshwater snails. II. East African Species. Danish Bilharziasis Laboratory, Charlottenlund

    Google Scholar 

  • Locke SA, McLaughlin JD, Dayanandan S, Marcogliese DJ (2010a) Diversity and specificity in Diplostomum spp. metacercariae in freshwater fishes revealed by cytochrome c oxidase I and internal transcribed spacer sequences. Int J Parasitol 40:333–343

    Article  CAS  PubMed  Google Scholar 

  • Locke SA, Mclaughlin JD, Marcogliese DJ (2010b) DNA barcodes show cryptic diversity and a potential physiological basis for host specificity among Diplostomoidea (Platyhelminthes: Digenea) parasitizing freshwater fishes in the St. Lawrence River, Canada. Mol Ecol 19:2813–2827

    Article  CAS  PubMed  Google Scholar 

  • Locke SA, Mclaughlin JD, Lapierre AR, Johnson PTJ, Marcogliese DJ (2011) Linking larvae and adults of Apharyngostrigea cornu, Hysteromorpha triloba, and Alaria mustelae (Diplostomoidea: Digenea) using molecular data. J Parasitol 97:846–851

    Article  PubMed  Google Scholar 

  • Moema EBE, King PH, Rakgole JN, Baker C (2013) Descriptions of diplostomid metacercariae (Digenea: Diplostomidae) from freshwater fishes in the Tshwane area. Onderstepoort J Vet Res 80:1–7

    Article  Google Scholar 

  • Moszczynska A, Locke SA, Mclaughlin JD, Marcogliese DJ, Crease TJ (2009) Development of primers for the mitochondrial cytochrome coxidase Igene in digenetic trematodes (Platyhelminthes) illustrates the challenge of barcoding parasitic helminths. Mol Ecol Resour 9:75–82

    Article  CAS  PubMed  Google Scholar 

  • Mukaratirwa S, Kristensen TK, Siegismund HR, Chandiwana SK (1998) Genetic and morphological variation of populations belonging to the Bulinus truncatus/tropicuscomplex (Gastropoda: Planorbidae) in South Western Zimbabwe. J Moll Stud 64:435–446

    Article  Google Scholar 

  • Musiba MJ, Nkwengulila G (2006) Occurrence of metacercariae of Diplostomum and Tylodelphys species (Diplostomidae) in Clarias species (Clariidae) from Lake Victoria. Tan J Sci 32:89–98

    Google Scholar 

  • Mwita C, Nkwengulila G (2004) Parasites of Clarias gariepinus (Butchell, 1822) from the Mwanza Gulf, Lake Victoria. Tan J Sci 30:53–62

    Google Scholar 

  • Nazmi M (1932) LIX.—Diplostomum Tregenna, sp. n., a new trematode parasite of the Egyptian Kite. J Nat Hist 9:567–573

    Article  Google Scholar 

  • Niewiadomska K (1986) Verification of the life-cycles of Diplostomum spathaceum (Rudolphi, 1819) and D. pseudospathaceum Niewiadomska, 1984 (Trematoda, Diplostomidae). Syst Parasitol 8:23–31

    Article  Google Scholar 

  • Niewiadomska K (1996) The genus Diplostomum—taxonomy, morphology and biology. Acta Parasitol 41:55–66

    Google Scholar 

  • Nkwengulila G, Kigadye ESP (2005) Occurrence of digenean larvae in freshwater snails in the Ruvu Basin, Tanzania. Tan J Sci 31:23–30

    Google Scholar 

  • Nolan MJ, Cribb TH (2005) The use and implications of ribosomal DNA sequencing for the discrimination of digenean species. Adv Parasitol 60:101–163

    Article  PubMed  Google Scholar 

  • Otachi EO, Locke SA, Jirsa F, Fellner-Frank C, Marcogliese DJ (2015) Morphometric and molecular analyses of Tylodelphys sp. metacercariae (Digenea: Diplostomidae) from the vitreous humour of four fish species from Lake Naivasha, Kenya. J Helminthol 89:404–414

    Article  CAS  PubMed  Google Scholar 

  • Overstreet RM, Curran SS, Pote LM, King DT, Blend CK, Grater WD (2002) Bolbophorus damnificus n. sp. (Digenea: Bolbophoridae) from the channel catfish Ictalurus punctatus and American white pelican Pelecanus erythrorhynchos in the USA based on life-cycle and molecular data. Syst Parasitol 52:81–96

    Article  PubMed  Google Scholar 

  • Pina S, Tajdari J, Russell-Pinto F, Rodrigues P (2009) Morphological and molecular studies on life cycle stages of Diphtherostomum brusinae (Digenea: Zoogonidae) from Northern Portugal. J Helminthol 83:321–331

    Article  CAS  PubMed  Google Scholar 

  • Pylkkö P, Suomalainen LR, Tiirora M, Valtonen ET (2006) Evidence of enhanced bacterial invasion during Diplostomum spathaceum infection in European Grayling, Thymallus thymallus (L.). J Fish Dis 29:79–86

    Article  PubMed  Google Scholar 

  • Quaggiotto EA, Valverde F (1992) New metacercariae of the genus Tylodelphys (Trematoda, Diplostomatidae) in lacustrine populations of Galaxias maculatus (Teleostei, Galaxiidae). Bol Chil Parasitol 47:19–24

    CAS  PubMed  Google Scholar 

  • Quaggiotto EA, Valverde F (1994) Larval stages of digenetic trematodes in Chilina sp. (Mollusca, Pulmonata) of some water bodies of Patagonia, Argentina. Bol Chil Parasitol 50:33–36

    Google Scholar 

  • Seppälä O, Karvonen A, Valtonen ET (2006) Susceptibility of eye fluke-infected fish to predation by bird hosts. Parasitology 132:575–579

    Article  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ukoli FMA (1968) Three new trematode parasites of the African Darter, Anhinga rufa rufa (Lacepéde and Daudin, 1802) in Ghana. J Helminthol 42:179–192

    Article  Google Scholar 

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Acknowledgments

This work was supported financially by the World Bank CIBI through the Faculty of Science, University of Dares Salaam, under the umbrella of the Science, Technology and Higher Education Project (STHEP), coordinated and implemented by the Ministry of Education and Vocational Training and the Ministry of Communication’s Science and Technology (MCST), a Natural Sciences and Engineering Research Council of Canada Discovery Grant A6979 to J. D. McLaughlin, and funding from the Canadian Genomics Research and Development Initiative to D. J. Marcogliese. We are also indebted to the Tanzania Fisheries Research Institute (TAFIRI) for granting us permission to use their laboratories. We thank Angela Rose Lapierre, who provided indispensable technical assistance, and an anonymous reviewer for helpful critical comments.

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Authors and Affiliations

  1. Department of Zoology and Wildlife Ecology, University of Dares Salaam, P.O. Box 35064, Dares Salaam, Tanzania

    F. D. Chibwana & G. Nkwengulila

  2. Department of Biology, University of Puerto Rico, Mayagüez, Puerto Rico, Box 9000, Mayagüez, PR, 00681-9000, USA

    S. A. Locke

  3. Department of Biology, Concordia University, 7141 Sherbrooke West, Montreal, Quebec, H4B 1R6, Canada

    J. D. McLaughlin

  4. Aquatic Contaminants Research Division, Water Science and Technology Directorate, Science and Technology Branch, Environment Canada, Montreal, Quebec, H2Y 2E7, Canada

    D. J. Marcogliese

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  1. F. D. Chibwana
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  2. G. Nkwengulila
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  3. S. A. Locke
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  4. J. D. McLaughlin
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  5. D. J. Marcogliese
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Correspondence to F. D. Chibwana.

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Chibwana, F.D., Nkwengulila, G., Locke, S.A. et al. Completion of the life cycle of Tylodelphys mashonense (Sudarikov, 1971) (Digenea: Diplostomidae) with DNA barcodes and rDNA sequences. Parasitol Res 114, 3675–3682 (2015). https://doi.org/10.1007/s00436-015-4595-8

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  • DOI: https://doi.org/10.1007/s00436-015-4595-8

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